The red fox (
Different habitats and diet composition strongly influence the helminth fauna of this wild carnivore (Barbosa
The red fox is also the definitive host of many intestinal parasitic species responsible for minor zoonosis, such as
The aim of the present study was to conduct an epidemiological survey on foxes’ intestinal parasites in a previously scarcely studied area of north-west Italy (Liguria and southern Piedmont). The purpose was to evaluate the risk of transmission not only among the foxes, but also to domestic animals (pets and livestock) and humans.
A total of 180 red foxes (107 males and 73 females) were obtained from 2009 to 2013 in the provinces of Imperia and Cuneo (north-west Italy). Foxes were culled according to the Italian law No. 157/92 and collected by a provincial office of the Veterinary Public Health Services (Section of Imperia of the Experimental Zooprophylactic Institute of Piedmont, Liguria and Aosta Valley, hereafter EZI). Individual data on the area of origin, gender, weight and age were recorded. The age of the animals was estimated on the basis of the general size of the body and of the dental development, as described by Harris (1978). Foxes were classified as “young” (1 year of age or less, n=45) or “adult” (more than 1 year of age, n=135).
Viscera were separated from the rest of the carcass during the necropsy at EZI and then transferred to the Parasitology Section of the Department of Veterinary Sciences, University of Pisa. The results of the examination of the extraintestinal viscera (cardiopulmonary system, stomach, kidneys, urinary bladder, liver and muscle tissues) are reported in Macchioni et al. (2013) and in Magi et al. (2015).
The intestines were frozen at -80°C for at least seven days for biosecurity reasons (inactivation of eggs of
Rectal faecal samples (at least 3g) were subjected to coprological analysis to detect parasitic eggs and larvae. Flotation in centrifuge with 50 % zinc sulfate (s.g 1.350) used as the flotation solutionaccording to the procedure described by Dryden
The specific identification of parasites was based on observation of the morphology of eggs, larvae or adult worms under light microscope and according to the taxonomic keys (Yamaguti 1959; Campbell, 1991). All parasites found were isolated, counted, separated by gender, and stored in 70 % alcohol.
Prevalences with 95 % confidence intervals (CI), mean abundance, mean intensity and range were calculated (Bush
The results of the examination of the intestine by SCT are shown in Table 1. The nematode species found were: Uncinaria stenocephala, Molineus legerae, Toxocara canis, Toxascaris leonina, Trichuris vulpis, Aonchotheca putorii, and Pterygodermatites affinis. The most prevalent cestodes belonged to the genus Mesocestoides, followed by cestodes from family Dilepididae and from the genus Taenia. On the basis of the morphologic and morphometric analyses of the scolex and of proglottids, most cestodes of the family Dilepididae were identified as Joyeuxiella spp. Regarding Taenia spp., only in four cases was it possible to identify the species on a morphological basis as T. polyacantha and T. pisiformis. All foxes were negative for E. multilocularis and E. granulosus. In two foxes trematodes were found and identifiend as belonging to the family Plagiorchidae. Epidemiological parameters are also shown in detail in Table 1.
Results of the intestinal examinations of 180 red foxes by SCT (% = prevalence; CI = 95% Confidence Interval; MA = Mean Abundance; MI = Mean Intensity; R = Range)
Intestinal parasites (180 foxes) | % | CI | MA | MI | R |
---|---|---|---|---|---|
70.0 | 63.3 - 76.7 | 5.56 | 7.9 | 1 – 62 | |
27.2 | 20.7 – 33.7 | 1.11 | 4.1 | 1 – 30 | |
26.7 | 20.2 – 33.1 | 1.07 | 4.0 1 | – 37 | |
25.6 | 19.2 - 31.9 | 2.00 | 7.8 | 1 – 50 | |
21.1 | 15.1 – 27.1 | 0.39 | 1.9 | 1 – 9 | |
8.9 | 4.7 – 13 | 0.69 | 7.8 | 1 – 35 | |
5.6 | 2.2 – 8.9 | 0.42 | 7.6 | 1 – 40 | |
81.7 | 76.0 - 87.3 | 44.44 | 54.4 | 10 – (~200) | |
Family Dilepididae | 29.4 | 22.8 – 36.1 | 5.55 | 18.8 | 5 – (~110) |
6.1 | 2.6 – 9.6 | 0.20 | 3.3 | 3 – 10 | |
1.1 | 0 – 2.6 | 0.03 | 3.0 | 1 – 3 | |
1.1 | 0 – 2.6 | 0.02 | 2.0 | 1 – 2 | |
1.1 | 0 – 2.6 | 0.02 | 2.0 | 1 – 3 |
Multiple intestinal infections were observed. Intracommunities consisting of three different helminths species were found in 30.9 % of examined foxes and subsequently two species in 22.4 %, four in 18.8 %, five in 12.1 %, as well as six in 1.8 % of the foxes. No fox was found completely negative for the intestinal helminths.
Comparing prevalences of intestinal parasites between age classes of the hosts, a significant difference was observed only for Mesocestoides spp. (P value of chi squared test= 0.021) and Pterygodermatites affinis (P value of Fisher’s exact test = 0.040) which showed a higher prevalence in adult foxes (> 1 year of age). In fact no significant differences in parasitic prevalences with respect to the gender were found. The presence of intestinal nematodes and cestodes is primarily determined by the fox feeding habits, which do not vary among gender (Artois, 1989; Richards et al., 1995; Vervaeke et al., 2005).
For the most prevalent nematode species (
Our study reveals that foxes in the study area host a wide variety of intestinal helminth species.
Table 2 shows the results of the coprological examination of 180 faecal samples by a flotation method. In order to assess the sensitivity (S) and specificity (S’) of the coprological test, the results of the coprological tests were compared with the intestinal examination by SCT that is considered as gold standard. While the specificity was high for both nematodes and cestodes (>0.95, with the exception of Ancylostomatidaes’= 0.83), the sensitivity was always lower. Values observed for nematodes were: Family Ancylostomatidae S=0.60;
Results of copromicroscopic examinations of faecal samples in 180 red foxes. The sensitivity (S), specificity (S’) of the coprological test was compared with the SCT results
Coproscopy with flotation (180 foxes) | % | CI | S | S’ |
---|---|---|---|---|
Ancylostomatidae | 47.2 | 39.9 – 54.5 | 0.60 | 0.83 |
18.3 | 12.5 – 23.8 | 0.56 | 0.95 | |
17.8 | 12.5 -23.8 | 0.51 | 0.95 | |
14.4 | 9.4 – 19.7 | 0.57 | 1.00 | |
7.2 | 3.0 -10.3 | 0.38 | 0.96 | |
4.4 | 1.7 – 8.0 | 0.19 | 0.99 | |
2.2 | 0.2 – 4.7 | 0.40 | 1.00 | |
. 1.1 | 0.0 – 0.28 | -- | -- | |
3.3 | 0.9 – 6.4 | 0.03 | 0.97 | |
2.8 | 0.5 – 5.5 | -- | -- | |
0.6 | 0.0 – 1.7 | 0.09 | 1.00 |
The present study confirms that red foxes in Liguria host many parasite species, as already reported in foxes in Italy and Europe. From a comparison of our results with those reported in other surveys, several observations can be drawn.
The second most common intestinal nematode was
The third most common intestinal helminth was
The prevalence of T. leonina in this study was higher than in most of the surveys presented in literature. In Slovenia a value of 2.5 % was found among 428 foxes examined (Vergles Rataj et al., 2013) and lower values were reported in Denmark (Saeed et al., 2006: 0.6 % of 1040 foxes) and in Romania (Barabási et al., 2010: 4.6 % of 561 foxes). However, in Switzerland a prevalence of 37.3 % was found among 228 foxes examined (Reperant et al., 2007). Since the transmission of T. leonina is mainly linked to the ingestion of a paratenic host (small mammals, birds, invertebrates) (Reperant et al., 2007) the prevalence observed in the study area could be due to the existence of these components in the diet of the foxes examined. This hypothesis is also supported by the high prevalence of Mesocestoides spp., which are typically linked to a predatory diet.
Although most human infections remain asymptomatic,
Cestodes belonging to the family Dilepididae in the present study were found with an overall prevalence of 29.4 %. Based on the morphological and morphometrical analyses of scolexes and proglottids most Dilepididae were identified as
The present study corroborates the frequent occurrence of false negative results from coprological examinations, while false positive results may be due to the ingestion of food contaminated with parasite eggs (i.e. pseudo-parasitism). The false negative results are possibly due to the small amount of faeces that can be recovered from foxes’ intestines or as a result of intermittent eggs excretion. Additionally some helminth eggs (ascarids and ancylostomids) in frozen faeces can modify their shape (Schurer
This implies that a single coprological examination of a subject may not be reliable and should always be repeated, using an appropriate flotation solution. In addition, coprological methods such as flotation may be coupled, when possible, with molecular diagnostic methods (Guardone
The present epidemiological study on intestinal helminths showed that the fox, in this scarcely studied area, hosts a wide range of helminth species of medical and veterinary importance. The absence of
The prevalence of zoonotic parasites in foxes in Liguria suggests the need to continue in the surveillance of these helminth species due to the increased proximity of foxes to humans and to domestic dogs with a significant public health implications (Deplazes
Considering that all parasitic species found in foxes are shared by dogs, the present epidemiological survey is also a source of valuable data on the epidemiology and diagnosis of parasitic species that are less known or probably underestimated in pets.
This research received no specific grant from any funding agency, commercial or not-for-profit sectors...
None.